Journal of Environmental Quality 30:1631-1635 (2001)
© 2001 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
TECHNICAL REPORT
Organic Compounds in the Environment
Oxidation of Phenolic Acid Derivatives by Soil and Its Relevance to Allelopathic Activity
Tsutomu Ohno*
Department of Plant, Soil and Environmental Sciences, Univ. of Maine, 5722 Deering Hall, Orono, ME 04469-5722
* Corresponding author (ohno{at}maine.edu)
Received for publication October 30, 2000.
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ABSTRACT
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Previous studies have suggested that phenolic acids from legume green manures may contribute to weed control through allelopathy. The objectives of this study were to investigate the oxidation reactions of phenolic acids in soil and to determine the subsequent effects of oxidation upon phytotoxicity. Soils were reacted for 18 h with 0.25 mmol L-1 benzoic and cinnamic acid derivative solutions and Mn release from the suspension was used as a marker for phenolic acid oxidation. The extent of oxidation in soil suspensions was in the order of 3,4-dihydroxy- > 4-hydroxy-3-methoxy- > 4-hydroxy- 
2-hydroxy–substituted benzoic and cinnamic acids. The same ranking was observed for cyclic voltammetry peak currents of the cinnamic acid derivatives. This suggests that the oxidation of phenolic acids is controlled by the electron transfer step from the sorbed phenolic acid to the metal oxide. A bioassay experiment showed that the 4-hydroxy-, 4-hydroxy-3-methoxy-, and 3,4-dihydroxy–substituted cinnamic acids were bioactive at 0.25 mmol L-1 concentration. Reaction with soil for 18 h resulted in the elimination of bioactivity of these three cinnamic acids at the 5% significance level. The oxidative reactivity of phenolic acids may limit the potential of allelopathy as a component of an integrated weed management system. However, the initial phytotoxicity after soil incorporation may coincide with the early, critical stage of weed emergence and establishment, so that allelopathic phenolic acids may still play a role in weed management despite their reactivity in soil systems.
Abbreviations: DI-H2O, deionized–distilled water • PhC, phenolic carbon
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INTRODUCTION
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CONCERNS regarding the adverse environmental effects of herbicide use have motivated the development of weed management practices that rely on ecological manipulations, rather than agrochemical usage. One such approach uses crop rotation strategies to utilize allelopathy as a component of an ecologically based weed control method (Liebman and Gallandt, 1997; Liebman and Ohno, 1997; Weston, 1996). Ohno et al. (2000) reported a 20% reduction in wild mustard (Sinapis arvensis L. subsp. arvensis) bioassay growth in soil–water extracts isolated 8 d after the field incorporation of red clover (Trifolium pratense L.) residue as compared with wheat (Triticum aestivum L.) stubble–amended control soils. This bioassay reduction was correlated most strongly with phenolic C in the soil–water extracts and suggests that red clover releases phenolics that inhibit the growth of certain weed species. Extracts collected at and past 21 d after incorporation expressed no phytotoxicity, which suggests that reaction with soil ameliorates the toxicity of the released compounds (Ohno et al., 2000).
Phenolics have been the subject of many allelopathic studies (Siqueira et al., 1991; Inderjit, 1996). Inderjit and Dakshini (1999) and Dalton (1999) have recently stressed the need to explicitly consider soil processes to make allelopathy research relevant to agricultural systems. Phenolic acids react abiotically with soils, possibly involving ligand exchange reactions, soil surface catalyzed oxidation, and/or incorporation into soil organic matter (Dalton et al., 1989). Other researchers have also reported that phenolic acids are rapidly sorbed and subsequently oxidized by soil (Makino et al., 1996; Lehmann et al., 1987). Ohno and First (1998) reported that sorption of phenolic acids was related to both organic matter and Mn oxide content of soils. Excitation–emission matrix fluorescence spectroscopic analysis of 0.25 mol L-1 citrate extract of soils reacted with phenolic acids for 18 h did not indicate the presence of phenolic acids in the extracted solution. This spectral evidence combined with increased Mn2+ concentrations in the soil–phenolic acid suspensions suggested that phenolic acids were being oxidized upon sorption to the soil (Ohno and First, 1998).
In addition to abiotic reactions of phenolic acids in soils, biotic processes also are involved in determining the fate of phenolic compounds. Schmidt and Ley (1999) proposed that carbon-limited soil organisms would rapidly mineralize phenolic compounds due to their higher energy content on a per weight basis than simple sugars. Pue et al. (1995) demonstrated the importance of biotic effects on allelopathy expression by experimentally increasing the inhibitory activity of p-coumaric acid by the addition of noninhibitory levels of glucose in a soil bioassay. Blum et al. (1999) review published studies that demonstrate that microbial activity will alter phenolic compounds in soil and subsequently alter the expressed level of phytotoxicity. Microorganisms also produce enzymes that catalyze oxidation and polymerization reactions of phenolic acids (Huang et al., 1999).
Lehmann et al. (1987) and Schmidt and Ley (1999) have speculated that phenolic acid reactivity in soils may hinder the expression of allelopathy in the field through abiotic reactions such as oxidation of the allelochemicals and through biotic mineralization of the allelochemicals prior to interacting with the target species. The objectives of this study were to (i) determine the effects of substituent groups of phenolic acids on the oxidation of these acids in soil and (ii) determine the effect of phenolic acid oxidation on bioactivity to wild mustard seedlings in a laboratory bioassay.
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MATERIALS AND METHODS
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Soil Characterization
A surface horizon of a Nicholville (coarse-silty, isotic, frigid Aquic Haplorthod) soil was sampled from the University of Maine (USA) Sustainable Agriculture Research Farm. The soil was passed through a 4-mm sieve to remove coarse fragments and root debris and then air-dried. Soil chemical characterization was conducted using the methods of the Northeast Coordinating Committee on Soil Testing (1995). The pH (1:1 soil to H2O) was 6.1, and a total C content of 21.3 g kg-1 was determined using a Leco (St. Joseph, MI) CN-2000 analyzer. The metal oxide content of Mn (0.15 g kg-1), Fe (4.98 g kg-1), and Al (6.35 g kg-1) was determined using the ammonium oxalate extraction method (Iyengar et al., 1981). The hydrometer method for particle-size analysis indicated that the soil contained 57% sand, 32% silt, and 11% clay fractions.
Soil–Phenolic Acid Reaction
Reaction conditions described by Ohno and First (1998) were used to investigate the oxidation reaction of phenolic acids with soil. An initial study with four benzoic acid derivatives (2-hydroxy-; 4-hydroxy-; 3,4-dihydroxy-; and 4-hydroxy-3-methoxy–substituted moieties) and four cinnamic acid derivatives with the same groups were screened for oxidative reactivity. Stock phenolic acid solutions of 2.50 mmol L-1 were made up by dissolving the reagent in deionized–distilled water (DI-H2O) with stepwise addition of 0.1 mol L-1 NaOH until pH 6.0 was reached. Phenolic acid solutions were diluted volumetrically to 0.25 mmol L-1 and were reacted with soil by shaking 5.00 g of soil with 25.0 mL of solution in a 50-mL centrifuge tube. This phenolic acid concentration is within the concentration range for typical soil solutions (Sposito, 1989). The control consisted of DI-H2O in place of the phenolic acid solution. The reaction was conducted at the native soil pH of 6.1. All treatments were replicated three times. The soil suspensions were agitated on an orbital-action shaker for 18 h at 20.0 ± 0.1°C. The tubes were then centrifuged at 900 x g for 30 min and the supernatant filtered through a 0.45-µm Nylaflo filter (Gelman Sciences, Ann Arbor, MI).
The concentrations of Mn and Fe in the extracts were determined using inductively coupled plasma–atomic emission spectrometry. Concentration of phenolic carbon (PhC) was determined by ultraviolet absorbance at the absorption maximum of each phenolic acid as determined from the spectra obtained from 220 to 400 nm using a 1-cm pathlength cell. Absorbance from the background organic matter was corrected by subtracting the absorbance at the specific wavelength in the DI-H2O control solutions.
The redox chemistry of the cinnamic derivatives in the absence of soil was investigated using cyclic voltammetry. This method uses a reversing, linear ramp of voltage potential over time to the working electrode (Brett and Brett, 1993). This allows the oxidation–reduction reactions of the analyte in the solution in the region surrounding the electrode. The current increases as the analyte electrode potential approaches the formal voltage of the redox couple and the reaction proceeds. At the stationary electrode, a concentration gradient of the electroactive analyte is formed as it is consumed by the redox reaction. Diffusion transport of analyte from bulk solution is slower than consumption leading to a decrease in current. In a simplified interpretation, the magnitude of current is related to the tendency of an analyte to undergo redox reactions. Deionized–distilled water was used to prepare 10 µmol L-1 phenolic acid in a 0.1 mol L-1 sodium acetate matrix, which was used to buffer pH at 5.8 and served as the supporting electrolyte. Cyclic voltammetry was conducted using a BAS (West Lafayette, IN) 100B/W analyzer. The cell setup consisted of a glassy carbon working electrode, a platinum auxiliary electrode, and an Ag|AgCl reference electrode. The solutions were degassed with argon prior to voltammetric analysis. The experimental conditions were: scanned voltage potential from 1.00 to -0.20 V with respect to the Ag|AgCl reference electrode; scan rate of 0.25 V s-1; and initial potential of 0.00 V.
Phenolic Acid Bioassay
The effects of oxidation of the four cinnamic acids investigated above, upon bioactivity, were investigated by using a laboratory bioassay. The bioassays were conducted at a phenolic acid concentration of 0.25 mmol L-1 (Yu and Matsui, 1997). The pH was buffered at 6.0 with 2-(4-morpholino)-ethanesulfonic acid and the Ca concentration was 3.0 mmol L-1. Twenty-five milliliter-aliquots of the phenolic acid solutions and of DI-H2O, which served as a control, were each reacted with 5.00 g of the Nicholville soil on an orbital shaker at 20.0 ± 0.1°C for 18 h. The suspensions were centrifuged at 900 x g for 30 min and filtered through a 0.2-µm Nylaflo filter. The phenolic acid and DI-H2O control solutions were also bioassayed without soil reaction to provide a reference bioassay value. All treatments were replicated three times and arranged in a randomized complete block design.
The bioassays used a standard phytotoxic methodology for allelochemicals as described by Macías et al. (2000). Bioassays were conducted in 100-mm-diameter Petri dishes lined with Whatman (Maidstone, England) No. 1 filter paper. Ten wild mustard seeds were distributed evenly in the Petri dishes and 5 mL of solution, filtered through 0.2-µm membrane filters from each replicate, was added to a Petri dish to obtain a dosage of 0.5 mL per seed. The individual Petri dishes were sealed with Parafilm to minimize evaporative loss of the solution. The dishes were placed in a dark incubator at 23.0 ± 0.1°C for 96 h and root length was recorded. The average root length for each Petri dish was selected for statistical analysis.
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RESULTS AND DISCUSSION
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Phenolic Acid Oxidation
The soil–water extract at 8 d after incorporation of red clover in an associated field study had less than 1% of PhC content that was released from the green manure, assuming that all of the water-soluble, plant-derived PhC was released (Ohno et al., 2000). In a companion field study, the concentration of Mn in soil–water extracts was higher in plots incorporated with clover than in control plots without clover, suggesting that plant-derived phenolic compounds are undergoing redox reactions resulting in release of soluble Mn2+ from Mn oxides present in the soil (Conklin, 2000). These observations suggest that sorption and oxidation (henceforth, referred to as oxidation for brevity) reactions of phenolic acids released from legume green manures are very important factors in the expression of phytotoxicity in the field.
A study with a suite of eight phenolic acids known to be allelopathic (Siqueira et al., 1991) demonstrated the strong influence of substitution moieties on the greater release of Mn and the lesser release of Fe from the soil to the solution (Table 1). Manganese release has been used as a marker for oxidation of phenolic acids by soil in a number of studies (Lehmann et al., 1987; Pohlman and McColl, 1986, 1989; Makino et al., 1996). Absorption spectra between 220 and 400 nm were recorded for the eight phenolic acids prior to and after the reaction with soil to monitor the phenolic acid reaction. Representative spectra for 2-hydroxycinnamic acid, which did not significantly release Mn or Fe into solution, and the spectra for 3,4-dihydroxycinnamic acid, which did release Mn and Fe into solution (Table 1), are shown in Fig. 1A and 1B, respectively. Spectral analysis of Fig. 1A and 1B can be used to detect oxidation of phenolic compounds due to changes in absorbance with oxidation (Stone and Morgan, 1984; Pohlman and McColl, 1989). The ratio of absorbance at 270:310 nm for 2-hydroxycinnamic acid, which did not release Mn to solution, was 1.75 ± 0.03 prior to soil reaction and 1.80 ± 0.04 after soil reaction, which were not significantly different at the 5% level. The 280:300 nm ratios for 3,4-dihydroxycinnamic acid were 1.03 ± 0.02 prior to and 1.21 ± 0.06 after soil reactions, which were significantly different at the 5% level. This independent signature of phenolic acid oxidation validates the use of Mn release as a surrogate marker for the oxidation process.
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Table 1. Release of Mn and Fe to the supernatant of the phenolic acid treatment and deionized–distilled water (DI-H2O) control after an 18-h reaction with the Nicholville soil.
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Fig. 1. Ultraviolet absorbance spectra of (A) 2-hydroxycinnamic acid and (B) 3,4-dihydroxycinnamic acid solutions prior to and after a 3-h reaction with soil. All spectra were corrected for background organic matter absorption by spectral subtraction of the deionized–distilled water (DI-H2O) control solution.
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The 26% reduction in absorbance at 270 nm for 2-hydroxycinnamic acid (Fig. 1A) despite no significant release of Mn or Fe over that of the DI-H2O control (Table 1) is probably the result of sorption by soil organic matter. There was a linear relationship between soil Mn release and the quantity of phenolic acid sorbed for the five phenolics that significantly released Mn (Fig. 2, filled symbols). Up to about 30% of the added phenolic acid may bind with the organic matter, thus showing a strong preference of the phenolic acid for organic matter sites or for organic matter–coated metal oxides over the metal oxide surface (Cheng, 1989). In addition to the abiotic sorption reaction, it is likely that some the phenolic acid lost from the solution phase was degraded by soil microbes present in the unsterilized soil used in this study.
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Fig. 2. Relationship between soil Mn release and phenolic acid sorption for the eight phenolic acids used in the study. The open symbols represent phenolic acids that did not significantly release soil Mn and the filled symbols represent phenolic acids that did significantly release soil Mn as shown in Table 1.
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Cyclic voltammetry was used to characterize the reduction–oxidation chemistry of the four cinnamic acid derivatives used in this study in the absence of soil. The peak currents for the compounds were: 1.2 µampere, 2-hydroxycinnamic acid; 3.3 µampere, 4-hydroxycinnamic acid; 15.8 µampere, 3-methoxy-4-hydroxycinnamic acid; and 66.2 µampere, 3,4-dihydroxycinnamic acid. The peak currents rank qualitatively in the same order as Mn and Fe release for the cinnamic acid derivatives shown in Table 1. There was a significant (p = 0.003) linear relationship between the cyclic voltammetry peak current and soil Mn release (Fig. 3). This suggests that the oxidation of the cinnamic acids and reduction of Mn oxides to soluble Mn2+ is being controlled by the electron transfer step from the sorbed phenolic acid to the metal oxide. Stone and Morgan (1984) reported that the kinetics of the formation of surface complexes between synthetic phenolic compounds and Mn oxides surfaces and the subsequent electron transfer step were the rate-determining steps in the oxidation reaction. The results shown in Fig. 2 and 3 extend the Stone and Morgan (1984) interpretation and show it to be applicable to native metal oxides found in soils as well.
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Fig. 3. Relationship between cyclic voltammetry peak current and soil Mn release for the four cinnamic acid derivatives used in the study.
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Oxidation Effects on Phytotoxicity
The results reported above support the speculation of Lehmann et al. (1987) and Schmidt and Ley (1999) that oxidation of phenolic acids may be relevant to allelopathy expression in soil systems by rapidly decreasing the concentration of allelopathic phenolic acids through biotic and abiotic oxidation processes. However, the products of the soil-induced oxidation may be themselves phytotoxic, which could result in either maintaining or increasing the phytotoxic effect. To gain further understanding of how phenolic acid oxidation may affect phytotoxicity, the cinnamic acid derivatives were selected for a bioassay study using wild mustard as a bioassay species.
The 4-hydroxy-, 4-hydroxy-3-methoxy-, and 3,4-dihydroxy–substituted cinnamic acids were bioactive as determined by significant root length differences at the 5% level from the root length of the DI-H2O control (Fig. 4). The length of roots exposed to 2-hydroxycinnamic acid were not significantly different from the control, indicating that this acid exhibited no effect upon the wild mustard seedlings. The 3,4-dihydroxycinnamic acid decreased root length whereas 4-hydroxycinnamic acid and 3-methoxy-4-hydroxycinnamic acid increased the root lengths. Visual assessment also revealed that these longer roots were smaller in diameter compared with the roots of the control or those exposed to 3,4-dihydroxycinnamic acid. Such differing physiological responses may indicate that these phenolic acids, which are similar chemically, may act in differing allelochemical modes.
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Fig. 4. Average root length for wild mustard seedlings exposed to the four cinnamic acid derivatives at 0.25 mmol L-1 concentration and deionized–distilled water (DI-H2O) control solutions with and without exposure to soil. CTL = DI-H2O control; 4-OH = 4-hydroxycinnamic acid; 2-OH = 2-hydroxycinnamic acid; 3-CH3O-4-OH = 4-hydroxy-3-methoxycinnamic acid; and 3,4-DiOH = 3,4-dihydroxycinnamic acid.
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The importance of the oxidation process on bioactivity is evident by comparing the bioactivity of the phenolic acids before and after reaction with the soil (Fig. 4). Upon reaction with soil, the bioassays of root growth from the three cinnamic acid derivatives that were previously bioactive were not significantly different from the level of the DI-H2O control. This indicates that soil reaction eliminates the bioactivity of these phenolic acids. These results directly affirm the speculation of Lehmann et al. (1987) and Schmidt and Ley (1999) that soil reactions, abiotic and biotic, are important in the expression of allelopathy in soil systems and that they may reduce the potential of allelopathy as a means of weed management under field conditions.
The findings of the study reported here may help explain why the phytotoxic effect of red clover cover crop incorporated into soil persists for less than 2 wk (Ohno et al., 2000). The phenolics that are released from the crop residue are either rapidly sorbed or sorbed with subsequent oxidation, which decreases the concentration of the phytotoxic phenolic compounds in the soil solution. This study's bioassay results indicate that the oxidized products are either not phytotoxic or else remain on the soil surface and do not interact with the plant roots. From an ecological perspective, the use of red clover incorporation as a component of integrated weed management may be limited due to sorption–oxidation processes that the phytotoxic compounds undergo in the soil system. However, the quantities of legume green manure residue that are typically incorporated may lead to elevated PhC concentrations in the initial stages of the growing season. In addition, from the weed-management viewpoint, phytotoxicity in the early growing season is the most desirable because weed populations earlier in the growing season are more likely to reduce crop yields than later-emerging weed populations (Liebman and Gallandt, 1997). Thus, allelopathy may still remain a viable component in the toolbox from which ecologically based weed management systems are designed.
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ACKNOWLEDGMENTS
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Support for this work was provided by agreement 96-35107-3274 of the USDA NRI Competitive Grants Program and Hatch funds from the Maine Agriculture and Forest Experiment Station.
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NOTES
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Maine Agric. and Forest Exp. Stn. Journal no. 2481.
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ABSTRACT
INTRODUCTION
